Original

Cunha GB et al. Article

/ Elastography of thyroid nodules in children http://dx.doi.org/10.1590/0100-3984.2018.0034

Elastography for the evaluation of thyroid nodules in pediatric

patients
A elastografia na avaliação de nódulos tireoidianos em pacientes pediátricos

Gustavo Bittar Cunha1,a, Luciana Cristante Izar Marino1,b, André Yamaya1,c, Cristiane Kochi1,d, Osmar Monte1,e,
Carlos Alberto Longui1,f, Adriano Namo Cury1,g, Eduardo de Faria Castro Fleury1,h
1. Irmandade da Santa Casa de Misericórdia de São Paulo, São Paulo, SP, Brazil.
Correspondence: Dr. Gustavo Bittar Cunha. Irmandade da Santa Casa de Misericórdia de São Paulo. Rua Doutor Cesário Mota Júnior, 112,
Vila Buarque. São Paulo, SP, Brazil, 01221-020. Email: gbittarcunha@gmail.com.
a. https://orcid.org/0000-0001-8014-1409; b. https://orcid.org/0000-0002-8257-3691; c. https://orcid.org/0000-0002-4454-6465;
d. https://orcid.org/0000-0003-2727-8646; e. https://orcid.org/0000-0002-2549-9237; f. https://orcid.org/0000-0002-6361-5235;
g. https://orcid.org/0000-0002-9777-8366; h. https://orcid.org/0000-0002-5334-7134.
Received 9 March 2018. Accepted after revision 28 May 2018.

How to cite this article:

Cunha GB, Marino LCI, Yamaya A, Kochi C, Monte O, Longui CA, Cury AN, Fleury EFC. Elastography for the evaluation of thyroid nodules in pediatric
patients. Radiol Bras. 2019 Mai/Jun;52(3):141–147.

Abstract Objective: To evaluate the usefulness of elastography (using manual compression) as an additional diagnostic tool for children and
adolescents with thyroid nodules.
Materials and Methods: This was a prospective study conducted between September 2012 and August 2013 at a hospital in Brazil.
We performed elastography, ultrasound, and fine-needle aspiration biopsy in 32 patients between 6 and 18 years of age who had,
in total, 38 thyroid nodules.
Results: The elastography findings correlated with the histopathological diagnosis in 78.5% of cases. In three patients, an unneces-
sary thyroidectomy could have been avoided if the elastography results had been prioritized. Only one malignant thyroid nodule was
found to show high elasticity.
Conclusion: Our results suggest that high elasticity of a nodule on elastography is associated with a low risk of thyroid cancer. If
further confirmed in other studies, elastography may prove useful as a complementary test for screening thyroid nodules in children.
Keywords: Thyroid neoplasms; Child; Thyroid nodule/diagnostic imaging; Elasticity imaging techniques; Ultrasonography.

Resumo Objetivo: Avaliar a utilidade da elastografia (usando compressão manual) como uma ferramenta adicional de diagnóstico em crian-
ças e adolescentes com nódulos da tireoide.
Materiais e Métodos: Este foi um estudo prospectivo realizado entre setembro de 2012 e agosto de 2013 em um hospital no
Brasil. Realizamos elastografia, ultrassonografia e biópsia por aspiração com agulha fina em 32 pacientes com idade entre 6 e 18
anos que tinham, no total, 38 nódulos tireoidianos.
Resultados: Os achados da elastografia em relação ao histopatológico foram corretos em 78,5% dos casos. A elastografia poderia
ter evitado a tireoidectomia desnecessária de três pacientes. Apenas um nódulo maligno da tireoide foi classificado como E1.
Conclusão: Nossos resultados sugeriram que a alta elasticidade de um nódulo na elastografia está associada a um baixo risco
de câncer de tireoide. Caso se confirme em outros estudos, a elastografia pode ser útil como teste de triagem complementar de
nódulos tireoidianos em crianças.
Unitermos: Neoplasias da tireoide; Criança; Nódulo da tireoide/diagnóstico por imagem; Técnicas de imagem por elasticidade;
Ultrassonografia.

INTRODUCTION
Thyroid nodules are rare in children, with an incidence
of 1.0–1.5%, although they are seen in up to 13% of adoles-
cents and young adults(1,2). However, the risk of malignancy
among children and adolescents with thyroid nodules is
high, the incidence of thyroid carcinomas in pediatric pa-
tients being 18.0–26.7%(3), with a risk of recurrence as high
as 39%(4). The incidence of thyroid cancer is 1:1,000,000
among children under 10 years of age, 1:200,000 among in-
dividuals 10–14 years of age and 1:75,000 among individu-
als 15–19 years of age. After puberty, girls are four times
more likely to have thyroid cancer than are boys, whereas
the female:male ratio is 1:1 in the prepubertal period(5).
Children are often diagnosed with advanced thyroid
cancer, 40–90% of cases presenting with lymph node in-
volvement and 20–30% presenting with distant metasta-
ses(6). A recent study of children with suspicious nodules
showed rates of malignancy and metastasis of 25% and
44%, respectively(7). Thorough investigation of suspicious
nodules that might require surgery is recommended to en-
sure early identification of malignancy and to avoid unnec-
essary thyroidectomy in those with benign nodules(8).

Radiol Bras. 2019 Mai/Jun;52(3):141–147 141

0100-3984 © Colégio Brasileiro de Radiologia e Diagnóstico por Imagem
Cunha GB et al. / Elastography of thyroid nodules in children
The protocol for the diagnosis of thyroid nodules in-
cludes physical examination, laboratory testing, fine-nee-
dle aspiration biopsy (FNAB), and thyroid ultrasound(2).
However, the most appropriate investigations of thyroid
nodules are still debated. Ultrasound is considered more
sensitive than physical examination for the detection of
thyroid nodules, although the former has low specificity for
differentiating between malignant and benign nodules(9).
The ultrasound criteria for malignant thyroid nodules in-
clude marked hypoechogenicity, indistinct or spiculated
margins, microcalcifications, intranodular vascularity, and
a taller-than-wide shape, although those criteria have a
wide range of sensitivities (55–95%) and specificities (52–
81%) for identifying and differentiating between malignant
or benign(10).
Although FNAB is thought to be the most accurate
method for diagnosing thyroid nodules, it is particularly dif-
ficult to perform the procedure in children because of the
discomfort associated with the biopsy. In addition, in 20–
40% of cases, the cytological findings following FNAB are
indeterminate or the specimen is insufficient for a definite
diagnosis. An accurate diagnosis is often made only after
histological evaluation(11). The nodule size that warrants a
biopsy is still debated. In adults, biopsy is recommended for
nodules ≥ 1.0 cm, whereas it is advisable to perform biopsy
on smaller nodules (those ≥ 0.5 cm) in children(2), because
of the high incidence of malignancy among children.
Elastography is a promising new technique for the
ultrasound evaluation of thyroid nodules(12,13). The tech-
nique relies on software that is available for conventional
ultrasound devices, and it evaluates the different types of
tissue, according to variations in their stiffness. It is based
on the principle that benign lesions are usually more elas-
tic than are malignant lesions, and elastography data can
facilitate the differential diagnosis of clinical pathologies,
such as thyroid nodules(14).
Ultrasound elastography is a noninvasive, painless
imaging tool, based on the estimation of the mechanical
properties (elasticity) of the tissue, that provides additional
and clinically relevant information(15). One recent study
showed that elastography can increase the accuracy of ul-
trasound in thyroid nodule differentiation and suggested
that it is the best noninvasive procedure available, com-
parable to FNAB for the evaluation of thyroid nodules,
regardless of the nodule size, provided that the nodule is
solid and without calcification(16).
Ultrasound elastography can be useful to distinguish
between benign and malignant thyroid nodules(16). Be-
cause malignant nodules exhibit stiffness on elastography,
this approach is also believed to have diagnostic value in
the identification of malignant lesions. In addition, re-
fined elastography approaches can provide an objective
ratio (or index) as a quantitative indicator to compare the
stiffness of a lesion with that of normal tissue or with a
direct power unit(17).
142
Elastography acquires information on the movement
of the tissue in response to the application of a small
amount of pressure(15). In softer tissues, the applied pres-
sure causes the tissue to compress more, whereas harder
tissues compress less(15). This compressibility of the tissue
(its stiffness) is known as strain and is presented as a color
map called an “elastogram”(15). Colors around and within
the nodules are evaluated and visually scored according to
the 4–5-scale scoring system, the regions of interest being
specified as the target region and the adjacent reference
region. A score of 4 indicates no elasticity in the target re-
gion (the nodule), and a score of 5 indicates no elasticity
in the target region or in the adjacent reference region (the
area showing posterior shadowing). The strain ratio is cal-
culated automatically, and a higher strain ratio translates
to a higher probability of malignancy(18). Another form of
evaluating the elastography data is by calculating the thy-
roid strain ratio to perform an objective, semiquantitative
analysis of the tissue stiffness(19).
Although many ultrasound elastography reports have
referred to “cytologically indeterminate” thyroid nodules,
it is practical to define the ultrasound indications for the
application of elastography during ultrasound scanning of
thyroid nodules(20). Elastography can be easily used as an
adjunctive noninvasive tool for B-mode ultrasound of inde-
terminate nodules, which are common(20,21). However, it is
not yet known whether this approach is suitable for the risk
stratification of such nodules(20,21).
In general, there are two ultrasound methods used
for determining thyroid nodule stiffness(22): strain elastog-
raphy, in which force is applied to the tissue by manual
compression and the tissue deformation is parallel to the
direction of the force; and shear-wave elastography (SWE),
in which a push beam is created and the tissue deforma-
tion is perpendicular to the direction of the force.
In children and adolescents with thyroid nodules, dif-
ferentiating between benign and malignant nodules is vi-
tally important. We evaluated the usefulness of strain elas-
tography as an additional diagnostic tool for children who
present with thyroid nodules.
MATERIALS AND METHODS
This was a prospective study conducted between Sep-
tember 2012 and August 2013 at a hospital in Brazil. The
research ethics committee of the institution approved the
study (Authorization no. 01687412200005479). The par-
ents or legal guardian of each participant gave written in-
formed consent, and all of the participants provided assent.
We evaluated 35 patients with thyroid nodules who had
been treated in the pediatric endocrinology department of
our hospital. In total, 42 thyroid nodules were identified on
physical examination or cervical ultrasound. We excluded
three patients with a total of four nodules: in one patient
(with two nodules), the FNAB results were inconclusive;
in another patient, the initial evaluation showed that the
Radiol Bras. 2019 Mai/Jun;52(3):141–147
Cunha GB et al. / Elastography of thyroid nodules in children
nodule had invaded the muscle but subsequent evaluations
showed that it had regressed; and one patient withdrew
from the study. Therefore, the final sample comprised 32
patients with a total of 38 thyroid nodules.
Laboratory evaluations of thyroid function (to deter-
mine circulating levels of thyroid-stimulating hormone,
free thyroxine, thyroid peroxidase antibody, antithyroglobu-
lin antibody, and calcitonin) were conducted. Patients with
euthyroidism were referred for ultrasound, elastography,
and FNAB. All examinations were conducted by the same
radiologist who, at the time of the study, had nine years
of experience in thyroid imaging. The specimen obtained
by FNAB was evaluated by a cytologist with more than 30
years of experience in cytological analysis.
The Bethesda System for Reporting Thyroid Cytopa-
thology was used in order to categorize the biopsy findings
as nondiagnostic (category I), benign (category II), atypia
of undetermined significance (category III), suspicious for
follicular neoplasm (category IV), suspicious for malig-
nancy (category V), or malignant (category VI). Thyroidec-
tomy was recommended for patients in whom the cytology
was potentially non-benign (thyroid nodules classified as
Bethesda category IV, V, or VI).
Ultrasound and elastography were performed on an
ultrasound system with a 5–14 MHz multifrequency trans-
ducer (Sonix SP; Ultrasonix Medical Corporation, Vancou-
ver, Canada). For the elastography study, we used special
software developed for the Ultrasonix system (version 3.0.2
[beta 1]; Ultrasonix Medical Corporation). The radiologist
in charge of the study obtained the rights to use the soft-
ware for experimental research during the study period.
Elastography was performed during the ultrasound exami-
nation, with the same real-time instrument and the same
Figure 1. Green light appears to the
left of the ultrasound image when
the degree of manual compression
is correct.
Radiol Bras. 2019 Mai/Jun;52(3):141–147
probe. The operator highlighted a box (region of interest)
that included the nodule to be evaluated.
The patient was placed in the supine position with the
neck in hyperextension, and the ultrasound transducer was
held perpendicular to the region of interest. For elastogra-
phy, slight, continuous manual compression was exerted
with the transducer on the thyroid nodules until resistance
could be felt. When resistance was sensed, the operator
relaxed the hand holding the transducer so as to provide
spontaneous decompression of the thyroid nodule. It is im-
portant that the pressure level remains constant through-
out the examination. The operator knows that the degree of
manual compression is correct when a green light appears
to the left of the ultrasound image, as shown in Figure 1.
The possibility to select the region of interest for the elas-
tography analysis allowed accurate screening, even of small
nodules, regardless of the position of the nodule within the
thyroid gland.
The principle of elastography is to acquire two ultra-
sound images (one before tissue compression and one af-
ter) and track tissue displacement by assessing the propa-
gation of the imaging beam. The use of dedicated software
allows tissue distortion to be measured accurately. This
technique is easy to perform. In the present study, exami-
nation times ranged from 30 s to 2 min. All examinations
were performed by the same operator, who was blinded to
the cytology results. The elastography software provides
elasticity information in various colors. In descending or-
der of elasticity, the colors are blue, green, yellow, and red.
In this study, elastography data were evaluated with a
scoring system, modified from the Azizi et al.(23) classifica-
tion, in which each thyroid nodule was given a score of E1
or E2. As illustrated in Figures 2, 3, and 4, if < 50% of a
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Cunha GB et al. / Elastography of thyroid nodules in children

nodule appeared in red, it was classified as E1 (elastic),

whereas a nodule in which > 50% of the area appeared in
red was classified as E2 (stiff).
The Bethesda cytology classification was used, and
thyroidectomy was recommended for patients with thyroid
nodules classified as Bethesda IV, V, or VI. McNemar’s test
was used in order to determine the level of agreement be-
tween the elastography findings (benign or malignant) and
the histological diagnosis.

RESULTS
Overview
Figure 2. Classification of thyroid nodules by elastography. A classification
of E1 indicated an elastic (probably benign) lesion, and a classification of E2 We enrolled 32 patients with one or more nodules,
indicated a hard (probably malignant) lesion. referred for suspicious nodules detected by palpation

Figure 3. Elastography image

of a thyroid nodule classified
as E1.

Figure 4. Elastography image

of a thyroid nodule classified
as E2.

144 Radiol Bras. 2019 Mai/Jun;52(3):141–147

Cunha GB et al. / Elastography of thyroid nodules in children
or as incidental radiographic findings. The mean age of
the patients was 12.9 years (range, 6–18 years) and the
female:male ratio was 2.5:1. The sample comprised 23 fe-
male patients and 9 male patients, with mean ages of 13.5
and 11.0 years, respectively.
The nodules ranged in size from 0.5 cm to 4.3 cm, and
all were submitted to FNAB. Of the 32 patients, 12 had
cytological abnormalities concerning for cancer and were
referred for total thyroidectomy. Overall, seven patients
were diagnosed with thyroid cancer, corresponding to an
incidence of 22%. The histological diagnosis was papillary
thyroid carcinoma in six of those patients and medullary
thyroid carcinoma in one.
The patients with cytologically benign nodules agreed
to long-term surveillance with annual cervical ultrasound
examinations. If there were changes in the ultrasound fea-
tures of a nodule, FNAB was again performed. At this writ-
ing, there have been no changes in the diagnosis of any of
the benign nodules.
The mean age of the seven patients diagnosed with
thyroid cancer was 12 years (range, 7–18 years). Six were
female and one was male. In the sample as a whole, the
test for antibodies was positive in 11 patients, only one of
whom was among those diagnosed with thyroid cancer.
The patient who was diagnosed with medullary thyroid car-
cinoma had elevated calcitonin levels: 3770 pg/mL (refer-
ence value: < 8.4 pg/mL).
Thyroid nodules
On the basis of the FNAB results, 24 (63%) of the 38
thyroid nodules were classified as Bethesda II, 6 (16%)
were classified as Bethesda IV, 7 (18%) were classified as
Bethesda V, and 1 (3%) was classified as Bethesda VI. All
thyroid nodules classified as Bethesda V and VI were found
to be malignant in the postoperative pathology. Of the six
thyroid nodules classified as Bethesda IV, five were benign
and one was malignant. Of the 38 thyroid nodules evalu-
ated, 18 (47%) were located in the right lobe; 17 (45%)
were located in the left lobe; 2 (5%) were located in the
isthmus; and 1 (3%) was diffuse. The two nodules in the
isthmus were both benign, whereas the nodule with a dif-
fuse appearance was malignant. Four of the nodules in the
right lobe were malignant, as were four of those in the left
lobe. All of the thyroid nodules (whether malignant or be-
nign) ranged in size from 1.3 cm to 1.6 cm.
Elastography features
Of the 14 thyroid nodules evaluated by histology,
5 (35.7%) were benign and 9 (64.3%) were malignant.
McNemar’s test showed that the elastography findings
correlated with the histopathological diagnosis in 78.5%
of the cases—in 21.4% of the benign nodules and 57.1%
of the malignant nodules. Only one malignant nodule
(the one diagnosed as medullary thyroid carcinoma) was
classified as E1. In that particular case, the patient had a
Radiol Bras. 2019 Mai/Jun;52(3):141–147
high level of calcitonin, as well as another thyroid nodule,
which was classified as Bethesda V. Of the five thyroid
nodules characterized as benign by histology, three were
classified as E1.
As in studies involving much larger samples (of
adults), the fact that the vast majority of patients with be-
nign cytology do not undergo surgery precludes an abso-
lute assessment of the accuracy of biopsy. However, of the
24 thyroid nodules characterized as benign after FNAB,
the elastography result was classified as E1 in 22 (92%).
Among the six patients referred for surgery after FNAB
findings suspicious for follicular neoplasm (Bethesda IV),
the elastography result was classified as E1 in three, and
the histology confirmed the thyroid nodules to be benign
in all three cases.
DISCUSSION
Although this study was carried out between Septem-
ber 2012 and August 2013, it is still of great importance
because there is a lack of articles evaluating the use of elas-
tography in thyroid nodules with a focus on children and
adolescents. Using elastography in real time, we observed
that thyroid nodules with greater elasticity are at a lower
risk of malignancy, as evidenced by the fact that three of
the five nodules with benign histology were classified as
E1. In addition, elastography classified only one malignant
nodule as E1. However, that patient had a final diagnosis
of medullary thyroid carcinoma, and it is known that up to
50% of such nodules exhibit greater elasticity(24).
Of the six patients with FNAB findings suspicious for
follicular neoplasm (Bethesda IV thyroid nodules), three
had elastography results classified as E1 and a histologi-
cal diagnosis of benign nodules. Therefore, those three pa-
tients were referred for thyroidectomy unnecessarily.
Although there have been a number of scientific re-
ports about the diagnostic value of elastography in adults,
only one study has addressed its use in children with thy-
roid nodules. In one recent study, Borysewicz-Sanczyk et
al.(25) employed elastography in their analysis of a total of
62 thyroid nodules in 47 children and adolescents: 37 fe-
males (age range, 9–18 years) and 10 males (age range,
7–17 years). The authors found elastography to have a high
negative predictive value for a benign diagnosis. The first
study to assess the role of elastography in the analysis of
thyroid nodules was conducted in 2007 by Rago et al.(16).
The authors reported a positive predictive value of 100%
and a negative predictive value of 98%. They concluded
that elastography is a useful adjunctive tool for the diagno-
sis of thyroid cancer.
If larger studies confirm our results, elastography might
allow children with elastic thyroid nodules to be placed
in follow-up without invasive procedures or unnecessary
thyroidectomies. However, the accuracy of elastography is
limited by intra- and inter-operator variability(26,27), which
could be minimized by using SWE techniques(28). Unlike
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Cunha GB et al. / Elastography of thyroid nodules in children
strain elastography, SWE is a quantitative technique that
is not operator-dependent, which avoids the limitations of
strain elastography in evaluations of the head and neck,
including the thyroid. Therefore, it is expected that SWE
can provide more information(28). However, to date, there
have been few studies aimed at standardizing specific val-
ues for the various SWE techniques used in the evaluation
of thyroid tissue(24).
In a recent study, Duan et al.(28) used two-dimensional
SWE ultrasound in the evaluation of 137 nodules smaller
than 10 mm, showing that SWE values were significantly
higher in malignant lesions than in benign lesions. The
SWE technique proved to be better than conventional
ultrasound in differentiating between malignant and be-
nign lesions. The combination of the two techniques had
a specificity of 94.5%, sensitivity of 95.7%, positive pre-
dictive value of 89.8%, and negative predictive value of
97.7%.
Fukuhara et al.(29), evaluating thyroid nodules with
SWE, showed that the “shear-wave velocity” was signifi-
cantly higher in papillary thyroid cancer than in normal
tissues and benign tumors, and there was no significant
difference between normal thyroid tissue and benign nod-
ules. The authors also found that the results were most
consistent for nodules larger than 20 mm.
In a large prospective study that evaluated 4550 nod-
ules, of which 1305 were evaluated with strain elastogra-
phy, the method showed a sensitivity of 74.2%, specificity
of 91.1%, negative predictive value of 98%, positive pre-
dictive value of 37.4%, and accuracy of 90% to differenti-
ate between malignant and benign nodules. In the present
study, we concluded that hard nodules should always be
considered suspicious for malignancy. However, nodules
that are “less stiff” are also frequently diagnosed as carci-
nomas(30).
CONCLUSION
Given the conflicts related to the small number of
studies addressing thyroid cancer in the pediatric popula-
tion, we thought it important to improve the investigation
of thyroid nodules in young patients. In the present study,
the low number of false-negative elastography results im-
plies that high elasticity of thyroid nodules is associated
with benign histology.
Although markers such as microRNAs and somatic
mutations of differentiated carcinomas have recently
shown accuracy in the evaluation of thyroid nodules, ul-
trasound elastography could be incorporated into the rou-
tine evaluation of thyroid nodules, with greater ease and
at a lower cost. However, further studies are needed in
order to strengthen the role of elastography in the pedi-
atric population, with a focus on FNAB cytology results
classified as Bethesda III or IV, because those categories
are responsible for the largest number of unnecessary thy-
roidectomies.
146
Acknowledgments
We are indebted to the patients and families evaluated,
as well as to Dr. Maria do Carmo Assunção Queiroz for her
expertise and assistance in the cytological analyses.
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